Abstract
Habitat loss and fragmentation would often induce delayed extinction, referred to as extinction debt. Understanding potential extinction debts would allow us to reduce future extinction risk by restoring habitats or implementing conservation actions. Although growing empirical evidence has predicted extinction debts in various ecosystems exposed to direct human disturbances, potential extinction debts in natural ecosystems with minimal direct human disturbance are little studied. Ongoing climate change may cause habitat loss and fragmentation, particularly in natural ecosystems vulnerable to environmental change, potentially leading to future local extinctions. Recent climate change would lead to extended growing season caused by earlier snowmelt in spring, resulting in expansion of shrubby species and thereby habitat loss and fragmentation of mountainous moorlands. We examined the potential extinction debts of species diversity and functional diversity (FD; trait variation or multivariate trait differences within a community) in subalpine moorland ecosystems subjected to few direct human disturbances. Plant species richness for all species and for moorland specialists were primarily explained by the past kernel density of focal moorlands (a proxy for spatial clustering of moorlands around them) but not the past area of the focal moorlands, suggesting potential extinction debt in subalpine moorland ecosystems. The higher kernel density of the focal moorland in the past indicates that it was originally surrounded by more neighborhood moorlands and/or had been locally highly fragmented. Patterns in current plant species richness have been shaped by the historical spatial configuration of moorlands, which have disappeared over time. In contrast, we found no significant relationships between the FD and historical and current landscape variables depicting each moorland. The prevalence of trait convergence might result in a less sensitive response of FD to habitat loss and fragmentation compared to that of species richness. Our finding has an important implication that climate change induced by human activities may threaten biodiversity in natural ecosystems through habitat loss and fragmentation.
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References
Alofs KM, González AV, Fowler NL (2014) Local native plant diversity responds to habitat loss and fragmentation over different time spans and spatial scales. Plant Ecol 215:1139–1151. https://doi.org/10.1007/s11258-014-0372-5
Bagaria G, Rodà F, Clotet M et al (2018) Contrasting habitat and landscape effects on the fitness of a long-lived grassland plant under forest encroachment: do they provide evidence for extinction debt? J Ecol 106:278–288. https://doi.org/10.1111/1365-2745.12860
Bommarco R, Lindborg R, Marini L, Öckinger E (2014) Extinction debt for plants and flower-visiting insects in landscapes with contrasting land use history. Divers Distrib 20:591–599. https://doi.org/10.1111/ddi.12187
Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540. https://doi.org/10.1111/j.1654-1103.2005.tb02393.x
Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58:445–449. https://doi.org/10.2307/1935620
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087. https://doi.org/10.1111/j.1365-2664.2011.02048.x
Carmona CP, Azcárate FM, de Bello F et al (2012) Taxonomical and functional diversity turnover in Mediterranean grasslands: Interactions between grazing, habitat type and rainfall. J Appl Ecol 49:1084–1093. https://doi.org/10.1111/j.1365-2664.2012.02193.x
Chapin FS III, McGuire AD, Randerson J et al (2000) Arctic and boreal ecosystems of western North America as components of the climate system. Glob Chang Biol 6(S1):211–223. https://doi.org/10.1046/j.1365-2486.2000.06022.x
Cornelissen JHC, Lavorel S, Garnier E et al (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380. https://doi.org/10.1071/BT02124
Cousins SAO, Vanhoenacker D (2011) Detection of extinction debt depends on scale and specialisation. Biol Conserv 144:782–787. https://doi.org/10.1016/j.biocon.2010.11.009
Daubenmire RF (1959) Canopy coverage method of vegetation analysis. Northwest Sci 33:43–64
Daimaru H, Yasuda M (2009) Global warming and mountain wet meadows in Japan. Chikyu Kankyo 14:175–182 ((in Japanese))
Diamond JM (1972) Biogeographic kinetics: Estimation of relaxation times for avifaunas of southwest pacific islands. Proc Natl Acad Sci USA 69:3199–3203. https://doi.org/10.1073/pnas.69.11.3199
Driscoll DA (2008) The frequency of metapopulations, metacommunities and nestedness in a fragmented landscape. Oikos 117:297–309. https://doi.org/10.1111/j.2007.0030-1299.16202.x
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419
Foley JA, Barford C, Coe MT et al (2005) Global consequences of land use. Science 309:570–574. https://doi.org/10.1126/science.1111772
Geospatial Information Authority of Japan (2000) The reports of changes in wetland area in Japan. https://www.gsi.go.jp/kankyochiri/shicchimenseki2.html. Accessed 8 Jan 2020.
González-Varo JP, Albaladejo RG, Aizen MA et al (2015) Extinction debt of a common shrub in a fragmented landscape. J Appl Ecol 52:580–589. https://doi.org/10.1111/1365-2664.12424
Gorham E (1991) Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl 1:182–195
Gorham E, Bayley SE, Schindler DW (1984) Ecological effects of acid deposition upon peatlands: a neglected field in “acid-rain” research. Can J Fish Aquat Sci 41:1256–1268
Gotelli NJ, McCabe DJ (2002) Species co-occurrence: a meta-analysis of J.M. Diamond’s assembly rules model. Ecology 83:2091–2096. https://doi.org/10.1890/0012-9658(2002)083[2091:SCOAMA]2.0.CO;2
Hájková P, Hájek M, Apostolova I (2006) Diversity of wetland vegetation in the Bulgarian high mountains, main gradients and context-dependence of the pH role. Plant Ecol 184:111–130. https://doi.org/10.1007/s11258-005-9056-5
Hanski I, Ovaskainen O (2002) Extinction debt at extinction threshold. Conserv Biol 16:666–673. https://doi.org/10.1046/j.1523-1739.2002.00342.x
Ibanez I, Katz DSW, Peltier D et al (2014) Assessing the integrated effects of landscape fragmentation on plants and plant communities: the challenge of multiprocess–multiresponse dynamics. J Ecol 102:882–895. https://doi.org/10.1111/1365-2745.12223
Jamin A, Peintinger M, Gimmi U et al (2020) Evidence for a possible extinction debt in Swiss wetland specialist plants. Ecol Evol 10:1–14. https://doi.org/10.1002/ece3.5980
Kamiyama C, Oikawa S, Kubo T, Hikosaka K (2010) Light interception in species with different functional groups coexisting in moorland plant communities. Oecologia 164:591–599. https://doi.org/10.1007/s00442-010-1674-5
Keith DA, Rodoreda S, Bedward M (2010) Decadal change in wetland–woodland boundaries during the late 20th century reflects climatic trends. Global Change Biol 16:2300–2306. https://doi.org/10.1111/j.1365-2486.2009.02072.x
Koyanagi T, Kusumoto Y, Yamamoto S et al (2009) Historical impacts on linear habitats: the present distribution of grassland species in forest-edge vegetation. Biol Conserv 142:1674–1684. https://doi.org/10.1016/j.biocon.2009.03.002
Krause B, Culmsee H, Wesche K, Leuschner C (2015) Historical and recent fragmentation of temperate floodplain grasslands: do patch size and distance affect the richness of characteristic wet meadow plant species? Folia Geobot 50:253–266. https://doi.org/10.1007/s12224-015-9220-1
Krauss J, Bommarco R, Guardiola M et al (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol Lett 13:597–605. https://doi.org/10.1111/j.1461-0248.2010.01457.x
Kudo G, Kawai Y, Amagai Y, Winkler DE (2017) Degradation and recovery of an alpine plant community: experimental removal of an encroaching dwarf bamboo. Alp Botany 127:75–83
Kuussaari M, Bommarco R, Heikkinen RK et al (2009) Extinction debt: a challenge for biodiversity conservation. Trends Ecol Evol 24:564–571. https://doi.org/10.1016/j.tree.2009.04.011
Laliberté E, Legendre P, Shipley B (2014) Package ‘FD’. Retrieved April 14th, 2020.
Lavorel S, Grigulis K, Lamarque P et al (2011) Using plant functional traits to understand the landscape distribution of multiple ecosystem services. J Ecol 99:135–147. https://doi.org/10.1111/j.1365-2745.2010.01753.x
Lindborg R, Eriksson O (2004) Historical landscape connectivity affects present plant species diversity. Ecol Soc Am 85:1840–1845. https://doi.org/10.1890/04-0367
Limpens J, Berendse F, Blodau C et al (2008) Peatlands and the carbon cycle: from local processes to global implications – a synthesis. Biogeosciences 5:1475–1491
Muraoka H, Takakura S (1988) Explanatory text of the geological map of the Hakkôda Geothermal area. Miscellaneous Map Series (No. 21–4), Geological Survey of Japan, Tsukuba, 27 p (in Japanese).
Nekola JC (2004) Vascular plant compositional gradients within and between Iowa fens. J Veg Sci 15:771–780. https://doi.org/10.1111/j.1654-1103.2004.tb02320.x
Noh J, Echeverría C, Pauchard A, Cuenca P (2019) Extinction debt in a biodiversity hotspot: the case of the Chilean Winter Rainfall-Valdivian Forests. Landsc Ecol Eng 15:1–12. https://doi.org/10.1007/s11355-018-0352-3
Olsen SL, Evju M, Endrestøl A (2018) Fragmentation in calcareous grasslands: species specialization matters. Biodivers Conserv 27:2329–2361. https://doi.org/10.1007/s10531-018-1540-z7,2329-2361
Otsu C, Iijima H, Nagaike T, Hoshino Y (2017) Evidence of extinction debt through the survival and colonization of each species in semi-natural grasslands. J Veg Sci 28:464–474. https://doi.org/10.1111/jvs.12514
Pakeman RJ, Lennon JJ, Brooker RW (2011) Trait assembly in plant assemblages and its modulation by productivity and disturbance. Oecologia 167:209–218
Parducci L, Bennett KD, Ficetola GF et al (2017) Ancient plant DNA in lake sediments. New Phytol 214:924–942
Pavoine S, Vallet J, Dufour A-B et al (2009) On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118:391–402. https://doi.org/10.1111/j.1600-0706.2009.16668.x
Pérez-Harguindeguy N, Díaz S, Garnier E et al (2013) New handbook for standardized measurement of plant functional traits worldwide. Aust J Bot 61:167–234. https://doi.org/10.1071/BT12225
Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758. https://doi.org/10.1111/j.1461-0248.2006.00924.x
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rao RC (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol 21:24–43. https://doi.org/10.1016/0040-5809(82)90004-1
Ramsar Convention Bureau (2002) What Is the Ramsar Convention on Wetlands? Ramsar Information Paper no. 2. Ramsar Convention Bureau, Gland. https://www.ramsar.org/sites/default/files/documents/library/info2007-02-e.pdf. Accessed 8 Jan 2020.
Rybicki J, Hanski I (2013) Species-area relationships and extinctions caused by habitat loss and fragmentation. Ecol Lett 16:27–38. https://doi.org/10.1111/ele.12065
Sasaki T, Katabuchi M, Kamiyama C et al (2013) Variations in species composition of moorland plant communities along environmental gradients within a subalpine zone in northern Japan. Wetlands 33:269–277. https://doi.org/10.1007/s13157-013-0380-6
Sasaki T, Katabuchi M, Kamiyama C et al (2014) Vulnerability of moorland plant communities to environmental change: Consequences of realistic species loss on functional diversity. J Appl Ecol 51:299–308. https://doi.org/10.1111/1365-2664.12192
Sasaki T, Katabuchi M, Kamiyama C et al (2012) Nestedness and niche-based species loss in moorland plant communities. Oikos 121:1783–1790. https://doi.org/10.1111/j.1600-0706.2012.20152.x
Sasaki T, Okubo S, Okayasu T et al (2009) Two-phase functional redundancy in plant communities along a grazing gradient in Mongolian rangelands. Ecology 90:2598–2608. https://doi.org/10.1890/08-1850.1
Satake Y, Hara H, Watari S, Tominari T (eds) (1989) Wild flowers of Japan: woody plants. Heibonsha, Tokyo, Japan ((in Japanese))
Satake Y, Ohwi J, Kitamura S, Watari S, Tominari T (eds) (1982) Wild flowers of Japan: herbaceous plants. Heibonsha, Tokyo, Japan ((in Japanese))
Semper-Pascual A, Macchi L, Sabatini FM et al (2018) Mapping extinction debt highlights conservation opportunities for birds and mammals in the South American Chaco. J Appl Ecol 55:1218–1229. https://doi.org/10.1111/1365-2664.13074
Sofaer HR, Skagen SK, Barsugli JJ et al (2016) Projected wetland densities under climate change: habitat loss but little geographic shift in conservation strategy. Ecol Appl 26:1677–1692. https://doi.org/10.1890/15-0750.1
Soga M, Koike S (2013) Mapping the potential extinction debt of butterflies in a modern city: implications for conservation priorities in urban landscapes. Anim Conserv 16:1–11. https://doi.org/10.1111/j.1469-1795.2012.00572.x
Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66. https://doi.org/10.1038/371065a0
Vitt DH, Chee W (1990) The relationship of vegetation to surface water chemistry and peat chemistry in fens of Alberta, Canada. Vegetatio 89:87–106. https://doi.org/10.1007/BF00032163
Wearn OR, Reuman DC, Ewers RM (2012) Extinction debt and windows of conservation opportunity in the Brazilian Amazon. Science 337:228–232. https://doi.org/10.1126/science.1219013
Wheeler BD, Proctor MCF (2000) Ecological gradients, subdivisions and terminology of north-west European mires. J Ecol 88:187–203. https://doi.org/10.1046/j.1365-2745.2000.00455.x
Acknowledgements
We thank our laboratory members for helping with field work, especially Yuki Iwachido, Misa Nambu, Issei Nishimura and Yutaro Yoshitake. We also thank Koji Yonekura for advice on species identification. This work was funded by Grant-in-Aid for Scientific Research B (no.18H02221 and no. 20H04380) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
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This work was funded by a Grant-in-Aid for Scientific Research B (nos. 18H02221 and 20H04380) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
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D.M and T.S conceived and designed the study. All authors collected the data. D.M. analyzed the data. D.M and T.S wrote the first draft of the manuscript. All authors contributed to the revisions.
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Makishima, D., Sutou, R., Goto, A. et al. Potential extinction debt due to habitat loss and fragmentation in subalpine moorland ecosystems. Plant Ecol 222, 445–457 (2021). https://doi.org/10.1007/s11258-021-01118-4
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DOI: https://doi.org/10.1007/s11258-021-01118-4